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Growing up in the Spy vs. Spy era, and a bit later in the Watergate age, I developed a keen appreciation for clandestine operations, which I assumed at that time were unique to human culture. As it turns out, eavesdropping is practiced by many different species for a variety of reasons. One important example occurs in bird flocks composed of several species of birds. Antshrikes (Thamnomanes ardesiacus) are sentinel species in multi-species flocks because they produce alarm calls when they spot a predacious raptor flying overhead, alerting other nearby birds of the threat. Ari Martinez and his colleagues wondered whether hanging out with antshrikes allowed these other bird species to expand their niches to forage in areas that might otherwise be too dangerous.

An antshrike perched in the Amazonian rainforest. Credit: E. Parra.

This fear-based niche shift hypothesis makes two related predictions. First, in the absence of antshrikes, the remainder of the flock should shift its range to areas with lower predation risk. Second, without antshrikes some birds might leave the flock entirely, because without sentinel services they no longer benefit from hanging with other birds. To test these predictions, Martinez and his colleagues identified eight flocks of 5-8 species (including antshrikes) in a tropical lowland forest in southeastern Peru. They established four removal flocks from which they removed all antshrikes after capturing them in mist nets. They left four control flocks, in which they captured all antshrikes, but then returned them to the flock (to control for the effects of handling).

Research team mist-netting and measuring antshrikes. Credit Micah Reigner

To determine where the flock was spending its time, researchers used a GPS device every 10 minutes to record the center of the flock. They also censused each flock for species composition from dawn to dusk for three days before removal and three days after removal. In control flocks, home range overlapped extensively (average of 69%) when comparing the first (pre-removal) and second (post-removal) three-day period. In removal flocks, there was only 8% overlap in home range, indicating that the remaining flock was shifting its range when antshrikes were gone.

Home ranges of a control flock (top) and a flock which had antshrikes removed (bottom). Red color indicates home range during the three day pre-removal period, while blue color indicates home range during the three day post-removal period. Deeper colors indicate greater occupancy.

But are the remaining species shifting their niches to safer locations when antshrikes are no longer available as sentinels? To answer this question the researchers measured the presence or absence of vegetation cover at different height intervals every 10 minutes at the center of the flock. Comparing the second (post-removal) to the first (pre-removal) period, the removal flocks (those without antshrikes) moved into understory vegetation (0-8 meters high) that was substantially denser than was the vegetation inhabited by the control flocks (those with antshrikes). Presumably, dense understory protects birds without sentinels from being spotted or captured by raptors flying overhead. These dense understory areas are usually associated with less tree cover at higher height intervals (above 16 meters), which allows more sunlight to reach the forest floor, resulting in lush vegetation growth.

Proportion change in vegetation cover occupied by flocks from pre-trial to post-trial period at different height intervals. Positive numbers indicate an increase in vegetation density. Error bars are 95% confidence intervals. Data are based on the behavior of four control and four removal flocks.

Flocking occurrence is the proportion of time individuals of a particular species spend in flocks. The fear-based niche shift hypothesis predicts that flocking occurrence should decrease when sentinel species are removed because the benefits of flocking are reduced for the remaining species. When the researchers compared post-removal to pre-removal time-periods, five species showed strong reductions in flocking occurrence for removal flocks in comparison to control flocks, two were unchanged, and one species showed an increase in flocking occurence.

The authors emphasize that though flocking occurrence decreased for most species, the flocks did remain intact, which indicates that there are probably other benefits from flocking besides the opportunity to eavesdrop. There might be safety in numbers – a decrease in individual mortality as group size increases, or the possibility that the remaining flock members do provide some information about imminent predator attacks.

Martinez and his colleagues conclude that sentinels help other bird species succeed in tropical rainforests, thriving in dangerous habitats where they might otherwise fear to tread. These species may provide important ecosystem services, such as dispersing seeds and eating herbivorous insects that threaten plants that are the foundation of these tropical ecosystems.

When John Terborgh began research at Cocha Cashu Biological Station in Peru back in 1974, he probably did not expect to still be working there 43 years later, doing research and publishing papers about the astounding species diversity in its tropical floodplain rainforest.

John Terborgh leans against a fallen tree that has created a gap in the forest canopy. Credit: Lisa Davenport.

One contributor to species diversity in tropical forests is treefall gaps, which form when a mature tree falls down, opening up a gap in the overhead canopy. The most obvious change associated with treefall gaps is an increase in light that reaches the canopy floor. In comparison to the closed canopy, treefall gaps may be dryer, warmer, have increased plant transpiration rates, and may host many different species that colonize the new environment.

Small treefall gap in a dense rainforest. Credit: Irina Skinner

While it’s clear that gaps influence the physical environment of the forest floor, it is not clear how a changed physical environment translates to biological diversity of the treefall gap community. Comparing treefall gaps to closed canopy communities, Terborgh and his colleagues explored this relationship.

First the researchers asked whether the seed rain into tree gap communities is different from the seed rain into closed canopy communities. Seed rain describes the types and abundance of seeds that are dispersed into communities. Usually seeds are blown into communities by the wind, or enter attached to the bodies or excrement of animals. Alternatively, some seeds are autochorous – self-dispersing, in some cases aided by a change in fruit shape that causes seeds to be ejected explosively.

To do this analysis Terborgh and his colleagues needed a systematic way to measure seed rain. The researchers set up a regularly-spaced grid of small containers (seed traps) that collected a portion of the seeds that entered the community. They also needed a way to describe whether the canopy was closed, somewhat open, or very open as in a treefall gap. For each seed trap they calculated a canopy cover index (CCI), which measured the amount of vegetation found at different levels directly above the traps. A value of 0 indicated no vegetation (a completely open canopy), while a value of 6 indicated dense vegetation at all levels (a completely closed canopy).

As the graphs below indicate, there were some dramatic differences between gaps and canopies. Note that the x-axis has been log-transformed so CCI = 1 transforms to a log(CCI) = 0, and a CCI = 6 transforms to log(CCI) = 0.778. All four major groups of animal seed dispersers dispersed many more seeds into closed canopy forest than into treefall gaps. The relationship between seed abundance and canopy cover was strikingly linear for primates and small arboreal animals. This makes sense, as these animals tend to sit on trees, and spread seeds either through defecation of already eaten fruit, or by eating fruits and inadvertently spilling some seeds in the process. So very few trees in treefall gaps translates to many fewer seeds in treefall gaps, with most (76%) being blown in by the wind.

The log abundance of potentially viable seeds (PV seeds on y-axes) collected in seed traps in relation to the log (canopy cover index) for six different types of seed dispersal agents/mechanisms.

Terborgh and his colleagues realized that differences in seed dispersal could profoundly influence the number and types of plants that were recruited into the population. Despite the scarcity of animals in tree fall gaps, most of the saplings (79%) that recruited into gaps were animal dispersed, whereas wind-dispersed species made up only 1% of the saplings.

Though species diversity was lower in tree fall gaps in comparison to the closed canopy, species composition (the types of species found there) was very different in treefall gaps. There were many species that recruited only under gaps, and were never found under a closed canopy. Interestingly, there is good evidence that the small treefall gaps in this study recruited a different set of tree species than do larger treefall gaps, which tend to recruit species that do best under conditions of very bright sunlight. Thus the researchers conclude that treefall gaps, small and large, offer a wide range of environmental conditions not found in the closed canopy, that ultimately help to promote astoundingly high tropical forest tree diversity.

I am a slow learner. Several times in the past few years I have paddled my canoe under a particular sycamore tree in the New River in Radford, Virginia. Each time I do so, I am greeted by large numbers of cormorant poop bombs dropped by the dozens of cormorants that seem to find that particular tree to their liking, and this particular canoeist not to their liking. Fortunately, cormorants have bad aim, but unfortunately it is not that bad.

Daniel Natusch and three other researchers wanted to know how an analogous form of nutrient enrichment from large colonies of nesting Metallic Starlings (Aplonis metallica) affects the nearby ecosystem in a tropical Australian rainforest. They were interested in this question because it was obvious that the ground below the nesting colony trees was basically devoid of vegetation; they describe it as “an open moonscape”, contrasting sharply with the thick rainforest nearby. Other studies have shown that nutrient enrichment from bird guano leads to increased vegetation density – so why is this ecosystem different?

Dan Natusch conducts herpetological research with his son Huxley. Credit: Jessica Lyons

The researchers compared the biological, chemical and physical environment underneath 27 different colony trees to the environment underneath a randomly chosen tree 100-200 meters from the colony tree. As expected, they found very little vegetation near colony trees, in contrast to relatively dense vegetation near the randomly chosen trees.

Vegetation cover (left) and number of live stems (right) in relation to distance from the colony or randomly chosen tree (Point 0 on X-axis). Negative numbers are downslope and positive numbers are upslope from the tree.

Soil analyses showed that the soils under the colony trees had much higher concentrations of important nutrients. For example, phosphorus levels were more than 30 times greater, and ammonium nitrogen was about four times greater under colony trees than under the randomly chosen trees. The researchers wondered whether these nutrient levels were so high that they were toxic to vegetation. That would account for the dead zone under the colony trees. An alternative hypothesis is that animals (pigs and turkeys in particular) may be attracted to these high nutrient areas under the colonies, and may either kill germinating plants by eating or trampling them.

To test both hypotheses, at the beginning of the breeding season the researchers covered a portion of the colony tree region with metal cages (exclosures) that prevented turkeys and pigs from gaining access. They discovered a much greater number of seedlings under the exclosures in comparison to the areas where turkeys and pigs could access the seedlings.

They concluded that nutrient levels were not toxic to seedlings, but that pigs and turkeys were either eating or trampling the seedlings as they emerge. As you can see, the number of exclosure seedlings dropped sharply in July, in part because rainfall declines sharply in June, which leads to high plant mortality, particularly in the unshaded dead zone. But in addition, feral pigs broke into all of the exclosures that summer to access the seedlings and the nutrient-rich soil.

Do these dead zones actually benefit the starlings in any way? One possible advantage is that dead zones prevent snakes from climbing nearby trees and vines to gain access to the nests that are located high in the canopy of the colony tree. However there is good evidence that colony trees suffer high mortality, as 10 of the 27 colony trees died within three years of the study. Trees that fall during the nesting period could lead to the failure of all of the nests within that colony tree.

Why do we find dead zones beneath colonies of Metallic Starlings, and increased plant growth rate, larger plant size and greater plant diversity beneath the colonies of several other bird colonies? Most previous studies have looked at sea-bird colonies on small islands that have few terrestrial herbivores, so germinating seedlings are relatively undisturbed. This study occurred in a continuous forest in tropical Australia, which harbored a large population of hungry herbivores. These contrasting findings show the important role of environmental context for understanding how ecological interactions will play out. Given that we humans are continually adding nutrients to our environment (through natural bodily function and when we fertilize our fields), we need to carefully consider the biotic and abiotic players in the ecosystem, so we can predict the effects we are having on the environment.